Biosurfactants of Lactobacillus helveticus for biodiversity inhibit the biofilm formation of Staphylococcus aureus and cell invasion
Abstract
Aim: This study aimed to evaluate the differences of biosurfactants produced by two Lactobacillus helveticus strains against the biofilm formation of Staphylococcus aureus in vitro and in vivo. Materials & methods: Scanning electron microscopy, Real time-quantitative PCR (RT-qPCR) and cell assay were used to analyze the inhibiting effect of biosurfactants against biofilm formation. Results & conclusion: Results showed that the biosurfactants have anti-adhesive and inhibiting effects on biofilm formation in vivo and in vitro. The biofilm-formative genes and autoinducer-2 signaling regulated these characteristics, and the biosurfactant L. helveticus 27170 is better than that of 27058. Host cell adhesion and invasion results indicated that the biosurfactants L. helveticus prevented the S. aureus invading the host cell, which may be a new strategy to eliminate biofilms.
Papers of special note have been highlighted as: • of interest; •• of considerable interest
References
- 1. . Purification and characterization of a serine protease secreted by Brevibacillus sp. KH3 for reducing waste activated sludge and biofilm formation. Bioresour. Technol. 102(22), 10,650–10,656 (2011). • The development of biofilm resistant strains and the development of alternative therapeutic agents.
- 2. . Biomolecular mechanisms of staphylococcal biofilm formation. Future Microbiol. 8(4), 509–524 (2013).
- 3. . MIC versus MBEC to determine the antibiotic sensitivity of Staphylococcus aureus in peritoneal dialysis peritonitis. Perit. Dial. Int. 30(6), 652–656 (2010).
- 4. . Antibiotic-loaded synthetic calcium sulfate beads for prevention of bacterial colonization and biofilm formation in periprosthetic infections. Antimicrob. Agents Chemother. 59(1), 111–120 (2015).
- 5. . Lycopene attenuates aluminum-induced hippocampal lesions by inhibiting oxidative stress-mediated inflammation and apoptosis in the rat. J. Inorg. Biochem. 193, 143–151 (2019).
- 6. Comparative analysis between biofilm formation and gene expression in Staphylococcus epidermidis isolates. Future Microbiol. 13, 415–427 (2018).
- 7. . Production of lipopeptide biosurfactant by a marine Nesterenkonia sp. and its application in food industry. Front. Microbiol. 8, 1138 (2017).
- 8. . Optimizing the production of the biosurfactant lichenysin and its application in biofilm control. J. Appl. Microbiol. 120(1), 99–111 (2016).
- 9. . Rhamnolipids from non-pathogenic Burkholderia thailandensis E264: physicochemical characterization, antimicrobial and antibiofilm efficacy against oral hygiene related pathogens. N. Biotechnol. 36, 26–36 (2017).
- 10. Influence of PDO Ragusano cheese biofilm microbiota on flavour compounds formation. Food Microbiol. 61, 126–135 (2017).
- 11. . Biofilm formation and ethanol inhibition by bacterial contaminants of biofuel fermentation. Bioresour. Technol. 196, 347–354 (2015).
- 12. . High production of erythritol from Candida sorbosivorans SSE-24 and its inhibitory effect on biofilm formation of Streptococcus mutans. Bioresour. Technol. 198, 31–38 (2015).
- 13. . Streptococcus sanguinis biofilm formation & interaction with oral pathogens. Future Microbiol. 13, 915–932 (2018).
- 14. . Biosurfactant from Lactococcus lactis 53 inhibits microbial adhesion on silicone rubber. Appl. Microbiol. Biotechnol. 66(3), 306–311 (2004).
- 15. . Strategies for the prevention of microbial biofilm formation on silicone rubber voice prostheses. J. Biomed. Mater. Res. Part B Appl. Biomater. 81(2), 358–370 (2007).
- 16. . Staphylococcal adhesion and host cell invasion: fibronectin-binding and other mechanisms. Front. Microbiol. 8, 2433 (2017).
- 17. . The influence of Lactobacillus acidophilus-derived surfactants on staphylococcal adhesion and biofilm formation. Folia Microbiol. (Praha) 53(1), 61–66 (2008). • Shows the function of surfactants produced by Lactobacillus acidophilus inhibited the biofilm formation, but not sure about the difference in the same strains.
- 18. RNA-Seq of Bacillus licheniformis: active regulatory RNA features expressed within a productive fermentation. BMC Genomics 14, 667 (2013).
- 19. . Antistaphylococcal and biofilm inhibitory activities of gallic, caffeic, and chlorogenic acids. Biofouling 30(1), 69–79 (2014).
- 20. . LuxS/AI-2 system is involved in antibiotic susceptibility and autolysis in Staphylococcus aureus NCTC 8325. Int. J. Antimicrob. Agents 41(1), 85–89 (2013).
- 21. . Staphylococcus aureus autoinducer-2 quorum sensing decreases biofilm formation in an icaR-dependent manner. BMC Microbiol. 12, 288 (2012). • he anti-adhesive properties of L. acidophilus biosurfactant was used against microorganisms, through the LuxS/AI-2 single sensing decreases biofilm formation.
- 22. Inhibitory effects of citral, cinnamaldehyde, and tea polyphenols on mixed biofilm formation by food-borne Staphylococcus aureus and Salmonella enteritidis. J. Food Prot. 77(6), 927–933 (2014).
- 23. . Validation of the 2-DeltaDeltaCt calculation as an alternate method of data analysis for quantitative PCR of BCR-ABL P210 transcripts. Diagn. Mol. Pathol. 15(1), 56–61 (2006).
- 24. Antimicrobial, anti-adhesive and anti-biofilm potential of biosurfactants isolated from Pediococcus acidilactici and Lactobacillus plantarum against Staphylococcus aureus CMCC26003. Microb. Pathog. 127, 12–20 (2019). • Purifies some microbes against Staphylococcus aureus biofilm-related infections.
- 25. . Anti-biofilm activities of quercetin and tannic acid against Staphylococcus aureus. Biofouling 29(5), 491–499 (2013).
- 26. . Host physiologic changes induced by influenza A virus lead to Staphylococcus aureus biofilm dispersion and transition from asymptomatic colonization to invasive disease. MBio 7(4), e01235-16 (2016).
- 27. . Streptococcus pneumoniae modulates Staphylococcus aureus biofilm dispersion and the transition from colonization to invasive disease. MBio 9(1), e02089-17 (2018).
- 28. . Murine immune response to a chronic Staphylococcus aureus biofilm infection. Infect. Immun. 79(4), 1789–1796 (2011).
- 29. . Suppression of the inflammatory immune response prevents the development of chronic biofilm infection due to methicillin-resistant Staphylococcus aureus. Infect. Immun. 79(12), 5010–5018 (2011).
- 30. . The inhibitory effect of a Lactobacillus acidophilus derived biosurfactant on biofilm producer Serratia marcescens. Iran J. Basic Med. Sci. 18(10), 1001–1007 (2015). • Uses the anti-adhesive properties of L. acidophilus biosurfactant against microorganisms responsible for infections.
- 31. . Lactobacillus Acidophilus-derived biosurfactant effect on GTFB and GTFC expression level in Streptococcus Mutans biofilm cells. Braz. J. Microbiol. 42(1), 330–339 (2011).
- 32. Characterization of biosurfactants produced by Lactobacillus spp. and their activity against oral streptococci biofilm. Appl. Microbiol. Biotechnol. 100(15), 6767–6777 (2016). •• Study on the biosurfactants against oral streptococci biofilm infection.
- 33. . Antimicrobial and antiadhesive properties of a biosurfactant isolated from Lactobacillus paracasei ssp. paracasei A20. Lett. Appl. Microbiol. 50(4), 419–424 (2010).
- 34. . Evaluation and functional characterization of a biosurfactant produced by Lactobacillus plantarum CFR 2194. Appl. Biochem. Biotechnol. 172(4), 1777–1789 (2014).
- 35. . Biological surfactants vs polysorbates: comparison of their emulsifier and surfactant properties. Tenside Surfact. Det. 55(4), 273–280 (2018).
- 36. Streptococcus mutans displays altered stress responses while enhancing biofilm formation by Lactobacillus casei in mixed-species consortium. Front. Cell. Infect. Microbiol. 7, 524 (2017).
- 37. AI-2 quorum sensing negatively regulates rbf expression and biofilm formation in Staphylococcus aureus. Int. J. Med. Microbiol. 307(4-5), 257–267 (2017).
- 38. Methylthioadenosine/S-adenosylhomocysteine nucleosidase (Pfs) of Staphylococcus aureus is essential for the virulence independent of LuxS/AI-2 system. Int. J. Med. Microbiol. 303(4), 190–200 (2013).
- 39. . Functional analysis of luxS in Staphylococcus aureus reveals a role in metabolism but not quorum sensing. J. Bacteriol. 188(8), 2885–2897 (2006).
- 40. . Gene regulation of rhamnolipid production in Pseudomonas aeruginosa–a review. Bioresour. Technol. 102(11), 6377–6384 (2011).
- 41. . The role of NF-kappaB and H3K27me3 demethylase, Jmjd3, on the anthrax lethal toxin tolerance of RAW 264.7 cells. PLoS ONE 5(3), e9913 (2010).
- 42. . Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274(13), 8405–8410 (1999).
- 43. . Influence of adhesion force on icaA and cidA gene expression and production of matrix components in Staphylococcus aureus biofilms. Appl. Environ. Microbiol. 81(10), 3369–3378 (2015).
- 44. . Coordinated regulation by AgrA, SarA, and SarR to control agr expression in Staphylococcus aureus. J. Bacteriol. 193(21), 6020–6031 (2011). • Uses biofilm-relative genes to study with the biosurfactants.
- 45. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl Acad. Sci. USA 104(19), 8113–8118 (2007).
- 46. . Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat. Rev. Microbiol. 12(1), 49–62 (2014).
- 47. . Staphylococcus aureus biofilm: a complex developmental organism. Mol. Microbiol. 104(3), 365–376 (2017).
- 48. . AlCl3 inhibits LPS-induced NLRP3 inflammasome activation and IL-1beta production through suppressing NF-kappaB signaling pathway in murine peritoneal macrophages. Chemosphere 209, 972–980 (2018).
- 49. . Exotoxins of Staphylococcus aureus. Clin. Microbiol. Rev. 13(1), 16–34 (2000).
- 50. . Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274(5294), 1859–1866 (1996).
- 51. . Alpha-toxin is required for biofilm formation by Staphylococcus aureus. J. Bacteriol. 185(10), 3214–3217 (2003).
- 52. . Red wines and flavonoids diminish Staphylococcus aureus virulence with anti-biofilm and anti-hemolytic activities. Biofouling 31(1), 1–11 (2015).
- 53. . Stilbenes reduce Staphylococcus aureus hemolysis, biofilm formation, and virulence. Foodborne Pathog. Dis. 11(9), 710–717 (2014).
- 54. . Temperature-dependent control of Staphylococcus aureus biofilms and virulence by thermoresponsive oligo(N-vinylcaprolactam). Biotechnol. Bioeng. 112(4), 716–724 (2015).
- 55. . Bioactivity of glycolipopeptide cell-bound biosurfactants against skin pathogens. Int. J. Biol. Macromol. 109, 971–979 (2018).
- 56. . Biosurfactants: potential applications in medicine. J. Antimicrob. Chemother. 57(4), 609–618 (2006). •• Reviews the importance of biosurfactants in the medicine, especially the research of probiotic inhibition of the biofilm.